An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

Elife. 2021 Mar 31:10:e64694. doi: 10.7554/eLife.64694.

Abstract

Adolescence is a critical time for the continued maturation of brain networks. Here, we assessed structural connectome development in a large longitudinal sample ranging from childhood to young adulthood. By projecting high-dimensional connectomes into compact manifold spaces, we identified a marked expansion of structural connectomes, with strongest effects in transmodal regions during adolescence. Findings reflected increased within-module connectivity together with increased segregation, indicating increasing differentiation of higher-order association networks from the rest of the brain. Projection of subcortico-cortical connectivity patterns into these manifolds showed parallel alterations in pathways centered on the caudate and thalamus. Connectome findings were contextualized via spatial transcriptome association analysis, highlighting genes enriched in cortex, thalamus, and striatum. Statistical learning of cortical and subcortical manifold features at baseline and their maturational change predicted measures of intelligence at follow-up. Our findings demonstrate that connectome manifold learning can bridge the conceptual and empirical gaps between macroscale network reconfigurations, microscale processes, and cognitive outcomes in adolescent development.

Keywords: adolescence; connectome; human; longitudinal; multi-scale; neurodevelopment; neuroimaging; neuroscience.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adolescent Behavior*
  • Adolescent Development*
  • Adult
  • Age Factors
  • Brain / diagnostic imaging
  • Brain / growth & development*
  • Brain / metabolism
  • Cognition
  • Connectome*
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Humans
  • Longitudinal Studies
  • Magnetic Resonance Imaging
  • Male
  • Models, Neurological
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neural Pathways / diagnostic imaging
  • Neural Pathways / growth & development*
  • Neural Pathways / metabolism
  • Neurogenesis*
  • Transcriptome
  • Young Adult

Substances

  • Nerve Tissue Proteins